ROS of Distinct Sources and Salicylic Acid Separate Elevated CO2-Mediated Stomatal Movements in Arabidopsis.

Jingjing He,Alistair M Hetherington,Ruo-Xi Zhang,Honggang Liu,Zhongming Liu,Dae Sung Kim,Peng Sun,Yun-Kuan Liang

doi:10.3389/fpls.2020.00542

Jingjing He, Alistair M Hetherington + Show 6 more

Open Access

https://doi.org/10.3389/fpls.2020.00542

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Abstract

Elevated CO2 (eCO2) often reduces leaf stomatal aperture and density thus impacts plant physiology and productivity. We have previously demonstrated that the Arabidopsis BIG protein distinguishes between the processes of eCO2-induced stomatal closure and eCO2-inhibited stomatal opening. However, the mechanistic basis of this action is not fully understood. Here we show that eCO2-elicited reactive oxygen species (ROS) production in big mutants was compromised in stomatal closure induction but not in stomatal opening inhibition. Pharmacological and genetic studies show that ROS generated by both NADPH oxidases and cell wall peroxidases contribute to eCO2-induced stomatal closure, whereas inhibition of light-induced stomatal opening by eCO2 may rely on the ROS derived from NADPH oxidases but not from cell wall peroxidases. As with JA and ABA, SA is required for eCO2-induced ROS generation and stomatal closure. In contrast, none of these three signals has a significant role in eCO2-inhibited stomatal opening, unveiling the distinct roles of plant hormonal signaling pathways in the induction of stomatal closure and the inhibition of stomatal opening by eCO2. In conclusion, this study adds SA to a list of plant hormones that together with ROS from distinct sources distinguish two branches of eCO2-mediated stomatal movements.

Highlights

Stomata formed by a pair of guard cells regulate gas exchanges between plants and the atmosphere
To test the hypothesis that reactive oxygen species (ROS) production has a central role to play in defining stomatal carbon dioxide (CO2) responses, we started by monitoring ROS levels in the big mutant and wild-type Col-0 (WT) plants using the fluorescence of H2-DCFDA
Around 30% extra ROS were induced by elevated CO2 (eCO2) treatments, but peels pre-treated with diphenylene iodonium (DPI) or salicylhydroxamic acid (SHAM) failed to exhibit significant ROS accumulation during eCO2 treatment (Figures 1C,D)

Summary

Introduction

Stomata formed by a pair of guard cells regulate gas exchanges between plants and the atmosphere. Guard cells sense and integrate both extra- and intracellular signals, such as light, temperature, carbon dioxide (CO2), plant hormones, leading to plant adaptive responses. The continuing rise of atmospheric CO2 can profoundly impact plant physiology and crop yield potential via stomata, as elevated CO2 (eCO2) concentration in the atmosphere reduces leaf stomatal aperture and density in many species including crop plants (Woodward, 1987; Assmann, 1993; Keenan et al, 2013; Xu et al, 2016). CO2 signaling starts from CO2 conversion to bicarbonate (HCO3−) by βCA1 (beta Carbonic Anhydrase 1) and βCA4, followed by activation of MATE type transporter RHC1 (Resistance to High CO2), MPK4 (Mitogen-Activated Protein Kinase 4) and MPK12, subsequently leading to inhibition of HT1 (High Leaf Temperature 1), which phosphorylates and inactivates OST1 (Open Stomata 1). Repression of HT1 facilitates S-type anion channel activation by OST1 to mediate the anion effluxes resulting in stomatal closure (Hashimoto et al, 2006; Hu et al, 2010; Tian et al, 2015; Hashimoto-Sugimoto et al, 2016; Hõrak et al, 2016; Jakobson et al, 2016; Tõldsepp et al, 2018; Zhang et al, 2018)

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